BioInvasions Records (2019) Volume 8, Issue 1: 87–95

CORRECTED PROOF

Rapid Communication First record of Monocorophium uenoi (Stephenson, 1932) (Crustacea: Amphipoda: Corophiidae) in the Bay of Biscay, French Atlantic coast

Benoit Gouillieux1,* and Cécile Massé2 1Université de Bordeaux, Station Marine d’Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France 2UMS 2006 AFB-MNHN-CNRS Patrimoine Naturel, Station Marine d’Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France Author e-mails: [email protected] (BG), [email protected] (CM) *Corresponding author

Citation: Gouillieux B, Massé C (2019) First record of Monocorophium uenoi Abstract (Stephenson, 1932) (Crustacea: Amphipoda: Corophiidae) in the Bay of The non-indigenous amphipod Monocorophium uenoi was recorded for the first Biscay, French Atlantic coast. time on the French Atlantic coast. This species has been collected in Arcachon Bay BioInvasions Records 8(1): 87–95, and Bidasoa Estuary as early as 2007, probably introduced with non-native oysters. https://doi.org/10.3391/bir.2019.8.1.09 A summary on its morphological characters and its current distribution is done, and Received: 30 April 2018 an updated identification key to Monocorophium species for European waters is Accepted: 16 October 2018 provided. Published: 12 February 2019 Key words: non-indigenous species, Peracarida, Corophiini, Arcachon Bay, Bidasoa Thematic editor: Cynthia McKenzie Estuary, Pacific oyster Copyright: © Gouillieux and Massé This is an open access article distributed under terms of the Creative Commons Attribution License Introduction (Attribution 4.0 International - CC BY 4.0). OPEN ACCESS. The genus Monocorophium Bousfield and Hoover, 1997 is represented by 4 species in European waters: M. acherusicum (Costa, 1853), M. insidiosum (Crawford, 1937), M. sextonae (Crawford, 1937) and M. uenoi (Stephenson, 1932) (Lincoln 1979; Bousfield and Hoover 1997; Faasse 2014). These species are native from European waters, except M. uenoi native from Japan, and M. sextonae which may have a South-West Pacific origin for some authors (Goulletquer et al. 2002). M. uenoi was recorded in The Netherlands in 2013 (Faasse 2014) – the first report from European waters. The present paper deals with M. uenoi record from the French Atlantic coast, which precedes the previous record.

Materials and methods Study area (Figure 1) Arcachon Bay is a 180 km² macrotidal coastal lagoon, connected to the Atlantic Ocean by a narrow channel and receives freshwater from Leyre River. The lagoon is characterized by large intertidal flats (115 km²) (Plus et al. 2010). Farms rearing the Pacific oyster Magallana gigas (Thunberg, 1793) occupy the deeper intertidal. Between 2007 and 2017, water temperature

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 87 First record of Monocorophium uenoi in the Bay of Biscay

Figure 1. Locations in Europe with records of Monocorophium uenoi. NL: The Netherlands. AB: Arcachon Bay. BE: Bidasoa Estuary. Black spot: Faasse 2014. Red stars: present study.

ranged from 4 to 25 °C and salinity ranged from 21 to 36 with an average of 16 ± 4 °C and 33 ± 2 (mean ± SD) respectively. Bidasoa Estuary represents the border between France and Spain in the South East of the Bay of Biscay. It is a short estuary with some feral oyster reefs. No shellfish or commercial port are present. Water temperature ranged from 12 to 22 °C and salinity ranged from 13 to 35 ppt with an average of 17 ± 4 °C and 31 ± 5 (mean ± SD) respectively. Environmental data (temperature and salinity) for both Arcachon Bay and Bidasoa Estuary were provided by the SOMLIT (Sevice d’Observation en Milieu LITtoral, a French coastal monitoring network: http://somlit. epoc.u-bordeaux1.fr/fr/).

Material examined Monocorophium uenoi was collected during benthic surveys, in Arcachon Bay and Bidasoa Estuary (Figure 1, Table 1). Specimens were examined with a Nikon SMZ 1500 stereomicroscope and a Nikon Eclipse E400 microscope with up to 112,5 and 400x magnifications (and transmitted light) respectively. Body length (BL) was measured with NIS-Elements

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 88 First record of Monocorophium uenoi in the Bay of Biscay

Table 1. Sampling details. N = number of specimens of Monocorophium uenoi collected in Pacific oyster reef. Site Station Latitude Longitude Date N MNHN depository MNHN-IU-2016-3430 Arcachon Bay Les Hosses 44.666667 −1.166667 May 2007–June 2008 135* (25 specimens) – Jacquet 44.666667 −1.083333 July 2014 26 – Arguin 44.583333 −1.233333 December 2017 6 – La Nègue 44.666667 −1.133333 September 2015 1 MNHN-IU-2016-3429 – Ile aux oiseaux Nord 44.683333 −1.166667 September 2015 20 (5 specimens) MNHN-IU-2016-3428 Bidasoa Estuary Station nautique 43.366667 −1.766667 October 2015 50 (20 specimens) * Specimens collected during Salvo (2010) thesis.

Analysis software from the anterior margin of head to the posterior end of telson. For Scanning Electron Microscope (SEM) studies, specimens were dehydrated in a graded ethanol series, critical point dried, sputter coated with gold and examined with a Hitachi TM3030Plus scanning electron microscope. Some specimens were deposited in the Muséum National d’Histoire Naturelle (MNHN, Paris) (Table 1).

Results Out of 238 specimens of Monocorophium uenoi collected, 72% were females, including ovigerous individuals, and 28% were males. Both in Arcachon Bay and Bidasoa Estuary, specimens were all collected in oyster reefs (Magallana gigas) between May 2007 and December 2017 (see Table 1).

Diagnose of male Monocorophium uenoi from Arcachon Bay (SW France) (Figure 2) Rostrum short, projecting slightly beyond lateral head lobes. Antenna 1 peduncle article 1 without lateral and with 3 ventral robust setae, without ventromedial process. Antenna 2 peduncle article 3 without robust seta; article 4 with 1 ventromedial robust seta and distoventral bidentate tooth; article 5 without robust seta, with 1 proximoventral and 1 distomedial process. Gnathopod 1 dactylus longer than palmar margin. Gnathopod 2 dactylus with 3 ventral teeth (tip of dactylus not counted as tooth). Urosome segment 1–3 fused. Uropod 1 inserted mainly laterally from lateral notches; peduncle with 1 distomedial robust seta. Uropod 2 inner ramus outer margin bare. Telson with 3 proximolateral setae and with 2 row of 4 robust setae tooth-like on the dorsodistal depression.

Female Sexually dimorphic characters based on adult females, Arcachon Bay (SW France), (Figure 3A–C). Rostrum shorter, not exceeding lateral head lobes. Antenna 1 peduncle article 1 with 1 lateral robust seta. Antenna 2 peduncle article 3 with 1 pair of robust setae; article 4 with row of 3 single robust setae, without

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 89 First record of Monocorophium uenoi in the Bay of Biscay

distoventral tooth; article 5 without proximoventral process and with 1 ventromedial robust seta.

Figure 2. Monocorophium uenoi (Stephensen, 1932), males specimens from Jacquet, Arcachon Bay, July 2014. A) Head and antenna dorsal view; B) antenna 1 article 1 mesial view; C) antenna 2 mesial view with article 4 proximal ventromedial robust seta (black arrow); D) antenna 2 article 4 distoventral teeth and article 5 proximal ventral process (black arrow); E–G) gnathopod 2 distal part of propodus and dactylus showing variability in dactylus teeth; H) gnathopod 1 distal part of propodus and dactylus; I) uropod 1 and 2 dorsal view; J) telson dorsal view. Scale bars: A–C, I: 0.2 mm; D–H, J: 0.05 mm. Photomicrographs by B. Gouillieux.

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 90 First record of Monocorophium uenoi in the Bay of Biscay

Figure 3. Monocorophium uenoi (Stephensen, 1932), females specimens from Jacquet, Arcachon Bay, July 2014; A) antenna 1 article 1 mesial view; B) antenna 2 mesial view; C) urosome dorsal view. Monocorophium acherusicum (Costa, 1853), specimens from Arcachon Bay; D) male antenna 1 article 1 mesial view; E) male antenna 2 mesial view; F) female antenna 2 mesial view; G) uropod 1 dorsal view. Monocorophium insidiosum (Crawford, 1937), male specimens from Bidasoa Estuary; H) head and antenna dorsal view showing medial process on antenna 1 article 1 (black arrow). Monocorophium sextonae (Crawford, 1937), male specimen from Arcachon Bay; I) antenna 1 article 1 mesial view; J) antenna 2 mesial view. Scale bars: A, D: 0.1 mm; B, C, E–J: 0.2 mm. Photomicrographs by B. Gouillieux.

Variability Based on 60 specimens from Arcachon Bay and Bidasoa Estuary (BL range: 1.7–6.2 mm). Antenna 1 peduncle article 1 with 0–2 (7%) or 3–4 (93%) ventral robust setae. Antenna 2 peduncle article 4 with (80%) or without (20%) ventromedial

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 91 First record of Monocorophium uenoi in the Bay of Biscay

robust setae. Gnathopod 2 dactylus with 2 (13%) or 3 (74%) teeth, or with no left/right symmetry (13%), third tooth sometimes difficult to see (Figure 2F). Number of robust setae on antenna 1 peduncle article 1 or number of gnathopod 2 dactylus teeth not significantly correlated to body length (Spearman, ρ = 0.22; p-value = 0.1)

Discussion Description of Monocorophium uenoi Monocorophium uenoi present specimens correspond to Stephenson (1932) and subsequent descriptions except for: (1) female antenna 1 article 1 with 1 medial robust seta (versus 4 or 5 for Nagata 1960); (2) female antenna 2 article 3 with 2 robust setae (versus 3 for Barnard 1952); (3) male antenna 2 peduncle article 5 with proximoventral process (versus without for Stephensen 1932 and Nagata 1960; with or without for Barnard 1952); (4) gnathopod 2 dactylus with 2 or 3 posterior teeth (versus 3 or 4 for Faasse 2014); (5) telson with 3 proximolateral setae and with 2 row of 4 robust setae tooth-like on the dorsodistal depression (versus 1 pair of proximolateral setae and 2 row of 3 robust setae tooth-like for Stephensen 1932). Bousfield and Hoover (1997) published a revision of Corophiidae from Pacific coast of North America with description of new genus and new species. In their Monocorophium key, some updating is required. According to Stephensen (1932), Barnard (1952), Faasse (2014) and to our own observations, M. uenoi present gnathopod 1 dactylus longer than palmar margin but not always significantly; gnathopod 2 dactylus with 2 to 4 posterior teeth; urosome with distinct lateral notch and uropod 1 not specially ventrally inserted. Thus, we propose to modify Bousfield and Hoover (1997) key as follows: 3. Rostrum (male) weak, not projecting beyond lateral head lobes; uropod 2, inner ramus, outer margin spines ...... 4 Rostrum (male) strong, projecting beyond lateral head lobes; uropod 2, inner ramus, outer margin bare ...... 6 And 6. Male rostrum short, projecting slightly beyond lateral head lobes; Female antenna 2 article 4 with row of single robust setae and uropod 2 outer ramus with outer marginal robust setae ...... M. uenoi Male rostrum long, tip projecting distinctly beyond lateral head lobes; female article 4 with pairs robust setae (if row of single robust setae, then uropod 2 outer ramus with outer margin bare) ...... 7

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 92 First record of Monocorophium uenoi in the Bay of Biscay

Ecology As in The Netherlands (Faasse 2014), M. uenoi in Arcachon Bay and Bidasoa Estuary was recorded from intertidal Pacific oyster reefs. In Japan, Chile, and the USA (California, Rhode Island), it was mainly recorded in subtidal areas of shallow water bays to 18 m. Occasionally, it was encountered in estuaries, tidal-pools or associated with algae, and described as a tube-dwelling preferring sandy habitats and Zostera meadows (Stephensen 1932; Barnard 1952, 1964, 1969; Nagata 1966; Barnard and Reish 1959; Reish and Barnard 1967; Gonzalez 1991; Aikins and Kikuchi 2001, 2002; Kanaya et al. 2015). The species tolerates wide range of environmental parameters, including temperature and salinity (Matsumasa and Kurihara, 1988; present study).

Introduction history and vector Monocorophium uenoi native range extends from Russian waters to Korea and China (Gurjanova 1951; Kim and Lee 2008; Lowry 2000; Ren 2012). The first introduction was recorded from 1946 in Newport Bay, California, U.S.A. (Carlon 1979, in Faasse 2014). Its distribution expanded from Monterey Bay (Barnard 1966), south to Chile (Gonzalez 1991), and the Gulf of Mexico (Escobar-Briones et al. 2002). In 2013, it was recorded in The Netherlands (Faasse 2014). The records of specimens in Arcachon Bay already in 2007 (Table 1) confirms Faasse’s (2014) suggestion that the Netherlands population originated “… from a European area where it has been introduced from the Pacific unnoticed”. It has been amply established that the importation and transfer of non-native oysters resulted in the introduction of numerous non-native species (Bachelet et al. 2009; Lavesque et al. 2013; Gouillieux 2017). Arcachon Bay is one of the principal oyster culture sites in France. With its older and more spatially widespread populations of M. uenoi, Arcachon Bay may serve as a “seed bank” for its secondary spread, by transfer of shellfish or shellfish farm equipment, or, as in the case of Bidasoa Estuary, possibly in fouling of recreational vessels.

Identification key to adult of Monocorophium species (ERMS area) Modified from Faasse (2014) 1. Antenna 2 article 4 with ventrodistal tooth (males) (Figure 2C–D) ...... 2 – Antenna 2 article 4 without ventrodistal tooth (females) (Figure 3B) ...... 5 2. Uropod 1 peduncle inner margin with only 1 distal robust seta (Figure 2I) ...... 3 – Uropod 1 peduncle inner margin with at least 3 robust setae (Figure 3G) ...... 4 3. Antenna 1 article 1 without medial process (Figure 2A); Gnathopod 2 dactylus with 2 to 4 teeth (Figure 2E–G) ...... M. uenoi

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 93 First record of Monocorophium uenoi in the Bay of Biscay

– Antenna 1 article 1 with medial process (Figure 3H); Gnathopod 2 dactylus with 3 or 4 teeth (as Figure 2F–G) ...... M. insidiosum 4. Antenna 1 article 1 with maximum of 3 robust setae (Figure 3D); Antenna 2 article 4 without robust setae, article 5 with process (rarely with small proximal robust seta) (Figure 3E); Gnathopod 2 dactylus with 2 or 3 teeth (as Figure 2E–G) ...... M. acherusicum – Antenna 1 article 1 with at least 4 robust setae (Figure 3I); Antenna 2 article 4 with 2 or 3 robust setae, article 5 without proximal and distal process (Figure 3J); Gnathopod 2 dactylus with 2 teeth (as Figure 2E) ...... M. sextonae 5. Antenna 2 article 4 with row of single robust setae (Figure 3B) ...... 6 – Antenna 2 article 4 with row of paired robust setae (Figure 3F) ...... 7 6. Uropod 1 peduncle inner margin with only 1 distal robust seta (Figure 3C) ...... M. uenoi – Uropod 1 peduncle inner margin with at least 3 robust setae (Figure 3G) ...... M. sextonae 7. Uropod 1 peduncle inner margin with at least 3 robust setae (Figure 3G); Gnathopod 2 dactylus with 2 or 3 teeth (as Figure2E–G) ...... M. acherusicum – Uropod 1 peduncle inner margin with only 1 distal robust seta (as Figure 3C); Gnathopod 2 dactylus with 3 or 4 teeth (as Figure 2F–G) ...... M. insidiosum

Acknowledgements

The Authors wish to thank Guy Bachelet (Université de Bordeaux) to allow us to examine his personal collection, the Biodiversity Platform of EPOC laboratory for all equipment available, Laure Corbari and Paula Martin-Lefevre (MNHN, Direction des collections, Paris) for their help to deposit specimens in the MNHN collections. Finally, we thank the two reviewers for their constructive comments.

References

Aikins S, Kikuchi E (2001) Studies on habitat selection by amphipods using artificial substrates within an estuarine environment. Hydrobiologia 457: 77–86, https://doi.org/10.1023/A: 1012261116232 Aikins S, Kikuchi E (2002) Grazing pressure by amphipods on microalgae in Gamo Lagoon, Japan. Marine Ecology Progress Series 245: 171–179, https://doi.org/10.3354/meps245171 Bachelet G, Blanchet H, Cotte M, Dang C, de Montaudouin X, de Moura Queiros A, Gouillieux B (2009) A round-the-world tour almost completed: first records of the invasive mussel Musculista senhousia in the North-east Atlantic (southern Bay of Biscay). Marine Biodiversity Records 2: 1–4, https://doi.org/10.1017/S1755267209001080 Barnard JL (1952) Some Amphipoda from Central California. The Wasmann Journal of Biology 10(1): 9–36 Barnard JL (1964) Marine Amphipoda of Bahia de San Quintin, Baja California. Pacific Naturalist 4(3): 55–140 Barnard JL (1966) Benthic Anphipoda of Monterey Bay, California. Proceedings of the United States National Museum 119: 1–41, https://doi.org/10.5479/si.00963801.119-3541.1 Barnard JL (1969) A biological survey of Bahia de Los Angeles Gulf of California, Mexico, IV. Benthic Amphipoda (Crustacea). Transactions of the San Diego Society of Natural History 15(13): 175–228 Barnard JL, Reish DJ (1959) Ecology of Amphipoda and Polychaeta of Newport Bay, California. Allan Hancock Foundation Publications, Occasional Paper 21: 1–106

Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 94 First record of Monocorophium uenoi in the Bay of Biscay

Bousfield EL, Hoover PM (1997) The amphipod superfamily Coropjioidea on the Pacific coast of North America. Part V. Family Corophiidae: Corophiinae, new subfamily. Systematics and distributional ecology. Amphipacifica 2(3): 67–140 Costa A (1853) Relazione sulla memoria del Dottor Achille Costa, di Ricerche su’ Crostacei Amfipodi del Regno di Napoli. Rendiconti della Societa Reale Borbonica, Accademia delle Scienze, new series 2: 167–178 Crawford GI (1937) A review of the Amphipod Genus Corophium with notes on the British species. Journal of the Marine Biological Assocaition of the United Kingdom 21: 589–630, https://doi.org/10.1017/S0025315400053753 Escobar-Briones E, Winfield I, Ortiz M, Gasca R, Suárez E (2002) Amphipoda. In: Llorente J, Morrone JJ (eds), Biodiversidad, taxonomía y biogeografía de artrópodos de México: Hacia una síntesis de su conocimiento. Volumen III. México: Comisión Nacional para el Conocimiento y uso de la Biodiversidad. Universidad Nacional Autónoma de México, pp 341–371 Faasse M (2014) The Pacific amphipod Monocorophium uenoi (Stephensen, 1932) introduced to The Netherlands (NE Atlantic). BioInvasions Records 3: 29–33, https://doi.org/10.3391/bir. 2014.3.1.05 Gonzalez E (1991) Actual state of gammaridean amphipoda taxonomy and catalogue of species from Chile. Hydrobiologia 223: 47–68, https://doi.org/10.1007/BF00047628 Gouillieux B (2017) New records of benthic amphipods, Jassa slatteryi Conlan, 1990 and Ampithoe valida Smith, 1873 (Crustacea: Peracarida: Amphipoda) for the Bay of Biscay, France, with morphological notes. Cahiers Bioliologie Marine 58: 279–289 Goulletquer P, Bachelet G, Sauriau PG, Noel P (2002) Open Atlantic coast of Europe – A century of introduced species into French waters. In: Leppäkoski E, Gollasch S, Olenin S (eds), Invasive Aquatic Species of Europe. Kluwer Academic Publishers, Netherlands, pp 246–290, https://doi.org/10.1007/978-94-015-9956-6_30 Gurjanova EF (1951) Bokoplavy morei SSSR i sopredelnykh vod (Amphipoda,Gammaridea). [Amphipods of the seas of USSR and adjacent waters (Amphipoda, Gammaridea)]. Opredeliteli po faune SSSR, Akademiya Nauk SSSR, 41: 1–1029 Kanaya G, Suzuki T, Kikuchi E (2015) Impacts of the 2011 Tsunami on sediment characteristics ans macrozoobenthic assemblages in a shallow eutrophic lagoon, Sendai Bay, Japan. PLoS ONE 10: e0135125, https://doi.org/10.1371/journal.pone.0135125 Kim YH, Lee KS (2008) Gammarideans Fauna (Crustacea: Amphipoda) from off Yeonggwang Korea. Basic Science Journal of Dankook University 14: 31–35 Lavesque N, Sorbe JC, Bachelet G, Gouillieux B, de Montaudouin X, Bonifacio P, Blanchet H, Dubois S (2013) Recent discovery of Paranthura japonica Richardson, 1909 (Crustacea: Isopoda: Paranthuridae) in European marine waters (Arcachon Bay, Bay of Biscay). BioInvasions Records 2: 215–219, https://doi.org/10.3391/bir.2013.2.3.07 Lincoln RJ (1979) British marine Amphipoda: Gammaridea. British Museum (Natural History), London, 658 pp Lowry JK (2000) Taxonomic status of amphipod crustaceans in the South China sea with a checklist of known species. The Raffles Bulletin of Zoology 8: 309–342 Matsumasa M, Kurihara Y (1988) Distribution patterns of benthic small crustaceans and the environmental factors in a brackish shallow-water lagoon, Gamo lagoon. Benthos Research 33/34: 33–41, https://doi.org/10.5179/benthos1981.1988.33 Nagata K (1960) Preliminary notes on benthic gammaridean amphipoda from the Zostera region of Mihara Bay, Seto Inland Sea, Japan. Publications of the Seto Marine Biological Laboratory 8: 163–182, https://doi.org/10.5134/174693 Nagata K (1966) Studies on marine Gammaridean Amphipoda of the Seto Inland Sea. IV. Publications of the Seto Marine Biological Laboratory 8: 327–348, https://doi.org/10.5134/ 175420 Plus M, Dalloyau S, Trut G, Auby I, de Montaudouin X, Emery E, Noel C, Viala C (2010) Long-term evolution (1988-2008) of Zostera spp. meadows in Arcachon Bay (Bay of Biscay). Estuarine, Coastal and Shelf Science 87: 357–366, https://doi.org/10.1016/j.ecss.2010.01.016 Reish DJ, Barnard JL (1967) The benthic Polychaeta and Amphipoda of Morro Bay, California. Proceedings of the United States National Museum 120: 1–26, https://doi.org/10.5479/si.009 63801.120-3565.1 Ren X (2012) Fauna Sinica. Invertebrata Vol. 43. Crustacea, Amphipoda, Gammaridea. Science Press, 651 pp Salvo F (2010) Approche comparée des populations naturelles et cultivées d'huître japonaise Crassostrea gigas dans une lagune macro-tidale (Bassin d’Arcachon): cycle biologique, relations trophiques et effets sur le benthos. PhD Thesis, Université Bordeaux 1, 510 pp Stephensen K (1932) Some new amphipods from Japan. Zoological Museum, Copenhagen 487–501 Thunberg CP (1793) Tekning och Beskrifning på en stor Ostronsort ifrån Japan. Kongliga Vetenskaps Academiens Nya Handlingar 14(4–6): 140–142

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